Identification of an algal xylan synthase indicates that there is functional orthology between algal and plant cell wall biosynthesis
Abstract
Summary Insights into the evolution of plant cell walls have important implications for comprehending these diverse and abundant biological structures. In order to understand the evolving structure–function relationships of the plant cell wall, it is imperative to trace the origin of its different components. The present study is focused on plant 1,4‐β‐xylan, tracing its evolutionary origin by genome and transcriptome mining followed by phylogenetic analysis, utilizing a large selection of plants and algae. It substantiates the findings by heterologous expression and biochemical characterization of a charophyte alga xylan synthase. Of the 12 known gene classes involved in 1,4‐β‐xylan formation, XYS 1/ IRX 10 in plants, IRX 7, IRX 8, IRX 9, IRX 14 and GUX occurred for the first time in charophyte algae. An XYS 1/ IRX 10 ortholog from Klebsormidium flaccidum , designated K. flaccidum XYLAN SYNTHASE ‐1 ( Kf XYS 1), possesses 1,4‐β‐xylan synthase activity, and 1,4‐β‐xylan occurs in the K. flaccidum cell wall. These data suggest that plant 1,4‐β‐xylan originated in charophytes and shed light on the origin of one of the key cell wall innovations to occur in charophyte algae, facilitating terrestrialization and emergence of polysaccharide‐based plant cell walls.
- Authors:
-
- Department of Plant Biology Michigan State University East Lansing MI 48823 USA, DOE Great Lakes Bioenergy Research Center Michigan State University East Lansing MI 48823 USA
- Department of Biochemistry University of Cambridge Cambridge CB2 1QW UK
- Carlsberg Research Laboratory 1799 Copenhagen V Denmark
- Complex Carbohydrate Research Center University of Georgia 315 Riverbend Road Athens GA 30602 USA, BioEnergy Science Center Oak Ridge National Lab Laboratory Oak Ridge TN 37831 USA
- Complex Carbohydrate Research Center University of Georgia 315 Riverbend Road Athens GA 30602 USA
- Department of Plant and Environmental Sciences University of Copenhagen 1971 Frederiksberg C Denmark
- Botanical Institute Department of Biological Sciences Universität zu Köln Köln D‐50674 Germany
- BGI‐Shenzhen Beishan Industrial Zone Yantian District Shenzhen 518083 China
- Department of Plant Biology Michigan State University East Lansing MI 48823 USA, DOE Great Lakes Bioenergy Research Center Michigan State University East Lansing MI 48823 USA, Department of Biochemistry and Molecular Biology Michigan State University East Lansing MI 48824 USA
- Joint BioEnergy Institute Emeryville CA 94608 USA, Environmental Genomics and Systems Biology Division Lawrence Berkeley National Laboratory Berkeley CA 94720 USA
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1630145
- Alternate Identifier(s):
- OSTI ID: 1425434
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Published Article
- Journal Name:
- New Phytologist
- Additional Journal Information:
- Journal Name: New Phytologist Journal Volume: 218 Journal Issue: 3; Journal ID: ISSN 0028-646X
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; biosynthesis; cell wall; evolution; IRX10; Klebsormidium flaccidum; Klebsormidium nitens; xylan; XYS1
Citation Formats
Jensen, Jacob Krüger, Busse‐Wicher, Marta, Poulsen, Christian Peter, Fangel, Jonatan Ulrik, Smith, Peter James, Yang, Jeong‐Yeh, Peña, Maria‐Jesus, Dinesen, Malene Hessellund, Martens, Helle Juel, Melkonian, Michael, Wong, Gane Ka‐Shu, Moremen, Kelley W., Wilkerson, Curtis Gene, Scheller, Henrik Vibe, Dupree, Paul, Ulvskov, Peter, Urbanowicz, Breeanna Rae, and Harholt, Jesper. Identification of an algal xylan synthase indicates that there is functional orthology between algal and plant cell wall biosynthesis. United Kingdom: N. p., 2018.
Web. doi:10.1111/nph.15050.
Jensen, Jacob Krüger, Busse‐Wicher, Marta, Poulsen, Christian Peter, Fangel, Jonatan Ulrik, Smith, Peter James, Yang, Jeong‐Yeh, Peña, Maria‐Jesus, Dinesen, Malene Hessellund, Martens, Helle Juel, Melkonian, Michael, Wong, Gane Ka‐Shu, Moremen, Kelley W., Wilkerson, Curtis Gene, Scheller, Henrik Vibe, Dupree, Paul, Ulvskov, Peter, Urbanowicz, Breeanna Rae, & Harholt, Jesper. Identification of an algal xylan synthase indicates that there is functional orthology between algal and plant cell wall biosynthesis. United Kingdom. https://doi.org/10.1111/nph.15050
Jensen, Jacob Krüger, Busse‐Wicher, Marta, Poulsen, Christian Peter, Fangel, Jonatan Ulrik, Smith, Peter James, Yang, Jeong‐Yeh, Peña, Maria‐Jesus, Dinesen, Malene Hessellund, Martens, Helle Juel, Melkonian, Michael, Wong, Gane Ka‐Shu, Moremen, Kelley W., Wilkerson, Curtis Gene, Scheller, Henrik Vibe, Dupree, Paul, Ulvskov, Peter, Urbanowicz, Breeanna Rae, and Harholt, Jesper. Tue .
"Identification of an algal xylan synthase indicates that there is functional orthology between algal and plant cell wall biosynthesis". United Kingdom. https://doi.org/10.1111/nph.15050.
@article{osti_1630145,
title = {Identification of an algal xylan synthase indicates that there is functional orthology between algal and plant cell wall biosynthesis},
author = {Jensen, Jacob Krüger and Busse‐Wicher, Marta and Poulsen, Christian Peter and Fangel, Jonatan Ulrik and Smith, Peter James and Yang, Jeong‐Yeh and Peña, Maria‐Jesus and Dinesen, Malene Hessellund and Martens, Helle Juel and Melkonian, Michael and Wong, Gane Ka‐Shu and Moremen, Kelley W. and Wilkerson, Curtis Gene and Scheller, Henrik Vibe and Dupree, Paul and Ulvskov, Peter and Urbanowicz, Breeanna Rae and Harholt, Jesper},
abstractNote = {Summary Insights into the evolution of plant cell walls have important implications for comprehending these diverse and abundant biological structures. In order to understand the evolving structure–function relationships of the plant cell wall, it is imperative to trace the origin of its different components. The present study is focused on plant 1,4‐β‐xylan, tracing its evolutionary origin by genome and transcriptome mining followed by phylogenetic analysis, utilizing a large selection of plants and algae. It substantiates the findings by heterologous expression and biochemical characterization of a charophyte alga xylan synthase. Of the 12 known gene classes involved in 1,4‐β‐xylan formation, XYS 1/ IRX 10 in plants, IRX 7, IRX 8, IRX 9, IRX 14 and GUX occurred for the first time in charophyte algae. An XYS 1/ IRX 10 ortholog from Klebsormidium flaccidum , designated K. flaccidum XYLAN SYNTHASE ‐1 ( Kf XYS 1), possesses 1,4‐β‐xylan synthase activity, and 1,4‐β‐xylan occurs in the K. flaccidum cell wall. These data suggest that plant 1,4‐β‐xylan originated in charophytes and shed light on the origin of one of the key cell wall innovations to occur in charophyte algae, facilitating terrestrialization and emergence of polysaccharide‐based plant cell walls.},
doi = {10.1111/nph.15050},
journal = {New Phytologist},
number = 3,
volume = 218,
place = {United Kingdom},
year = {Tue Feb 20 00:00:00 EST 2018},
month = {Tue Feb 20 00:00:00 EST 2018}
}
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Works referenced in this record:
The location of (1?3)-?-glucans in the walls of pollen tubes of Nicotiana alata using a (1?3)-?-glucan-specific monoclonal antibody
journal, August 1991
- Meikle, P. J.; Bonig, I.; Hoogenraad, N. J.
- Planta, Vol. 185, Issue 1
Hemicelluloses
journal, June 2010
- Scheller, Henrik Vibe; Ulvskov, Peter
- Annual Review of Plant Biology, Vol. 61, Issue 1
Phylotranscriptomic analysis of the origin and early diversification of land plants
journal, October 2014
- Wickett, Norman J.; Mirarab, Siavash; Nguyen, Nam
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 45
Monoclonal Antibodies to Plant Cell Wall Xylans and Arabinoxylans
journal, April 2005
- McCartney, Lesley; Marcus, Susan E.; Knox, J. Paul
- Journal of Histochemistry & Cytochemistry, Vol. 53, Issue 4
SALAD database: a motif-based database of protein annotations for plant comparative genomics
journal, October 2009
- Mihara, Motohiro; Itoh, Takeshi; Izawa, Takeshi
- Nucleic Acids Research, Vol. 38, Issue suppl_1
Xylan biosynthesis
journal, April 2014
- Rennie, Emilie A.; Scheller, Henrik Vibe
- Current Opinion in Biotechnology, Vol. 26
The charophycean green algae provide insights into the early origins of plant cell walls
journal, August 2011
- Sørensen, Iben; Pettolino, Filomena A.; Bacic, Antony
- The Plant Journal, Vol. 68, Issue 2
HMDB: a knowledgebase for the human metabolome
journal, January 2009
- Wishart, D. S.; Knox, C.; Guo, A. C.
- Nucleic Acids Research, Vol. 37, Issue Database
Correlative Imaging of Fluorescent Proteins in Resin-Embedded Plant Material 1
journal, March 2013
- Bell, Karen; Mitchell, Steve; Paultre, Danae
- Plant Physiology, Vol. 161, Issue 4
GUX1 and GUX2 glucuronyltransferases decorate distinct domains of glucuronoxylan with different substitution patterns
journal, March 2013
- Bromley, Jennifer R.; Busse-Wicher, Marta; Tryfona, Theodora
- The Plant Journal, Vol. 74, Issue 3
Why Plants Were Terrestrial from the Beginning
journal, February 2016
- Harholt, Jesper; Moestrup, Øjvind; Ulvskov, Peter
- Trends in Plant Science, Vol. 21, Issue 2
Data access for the 1,000 Plants (1KP) project
journal, October 2014
- Matasci, Naim; Hung, Ling-Hong; Yan, Zhixiang
- GigaScience, Vol. 3, Issue 1
Classification, Naming and Evolutionary History of Glycosyltransferases from Sequenced Green and Red Algal Genomes
journal, October 2013
- Ulvskov, Peter; Paiva, Dionisio Soares; Domozych, David
- PLoS ONE, Vol. 8, Issue 10
Structural, mutagenic and in silico studies of xyloglucan fucosylation in Arabidopsis thaliana suggest a water-mediated mechanism
journal, August 2017
- Urbanowicz, Breeanna R.; Bharadwaj, Vivek S.; Alahuhta, Markus
- The Plant Journal, Vol. 91, Issue 6
An unusual xylan in Arabidopsis primary cell walls is synthesised by GUX3, IRX9L, IRX10L and IRX14
journal, June 2015
- Mortimer, Jenny C.; Faria-Blanc, Nuno; Yu, Xiaolan
- The Plant Journal, Vol. 83, Issue 3
Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth
journal, January 1993
- Carpita, Nicholas C.; Gibeaut, David M.
- The Plant Journal, Vol. 3, Issue 1
Arabidopsis irregular xylem8 and irregular xylem9 : Implications for the Complexity of Glucuronoxylan Biosynthesis
journal, February 2007
- Peña, Maria J.; Zhong, Ruiqin; Zhou, Gong-Ke
- The Plant Cell, Vol. 19, Issue 2
Evolution of xylan substitution patterns in gymnosperms and angiosperms: implications for xylan interaction with cellulose
journal, June 2016
- Busse-Wicher, Marta; Li, An; Silveira, Rodrigo L.
- Plant Physiology
Cell wall evolution and diversity
journal, January 2012
- Fangel, Jonatan U.; Ulvskov, Peter; Knox, J. P.
- Frontiers in Plant Science, Vol. 3
Designer biomass for next-generation biorefineries: leveraging recent insights into xylan structure and biosynthesis
journal, November 2017
- Smith, Peter J.; Wang, Hsin-Tzu; York, William S.
- Biotechnology for Biofuels, Vol. 10, Issue 1
Site-Directed Mutagenesis of IRX9, IRX9L and IRX14 Proteins Involved in Xylan Biosynthesis: Glycosyltransferase Activity Is Not Required for IRX9 Function in Arabidopsis
journal, August 2014
- Ren, Yanfang; Hansen, Sara Fasmer; Ebert, Berit
- PLoS ONE, Vol. 9, Issue 8
Discovery of diversity in xylan biosynthetic genes by transcriptional profiling of a heteroxylan containing mucilaginous tissue
journal, January 2013
- Jensen, Jacob K.; Johnson, Nathan; Wilkerson, Curtis G.
- Frontiers in Plant Science, Vol. 4
The DUF579 domain containing proteins IRX15 and IRX15-L affect xylan synthesis in Arabidopsis: A DUF579 protein affects xylan accumulation
journal, February 2011
- Jensen, Jacob K.; Kim, Hoon; Cocuron, Jean-Christophe
- The Plant Journal, Vol. 66, Issue 3
Asparagus IRX9, IRX10, and IRX14A Are Components of an Active Xylan Backbone Synthase Complex that Forms in the Golgi Apparatus
journal, March 2016
- Zeng, Wei; Lampugnani, Edwin R.; Picard, Kelsey L.
- Plant Physiology, Vol. 171, Issue 1
Comparison of five xylan synthesis mutants reveals new insight into the mechanisms of xylan synthesis
journal, December 2007
- Brown, David M.; Goubet, Florence; Wong, Vicky W.
- The Plant Journal, Vol. 52, Issue 6
Evidence for land plant cell wall biosynthetic mechanisms in charophyte green algae
journal, September 2014
- Mikkelsen, Maria D.; Harholt, Jesper; Ulvskov, Peter
- Annals of Botany, Vol. 114, Issue 6
Rhamnogalacturonan I in Solanum tuberosum tubers contains complex arabinogalactan structures
journal, May 2004
- Øbro, Jens; Harholt, Jesper; Scheller, Henrik Vibe
- Phytochemistry, Vol. 65, Issue 10
Versatile High Resolution Oligosaccharide Microarrays for Plant Glycobiology and Cell Wall Research
journal, September 2012
- Pedersen, Henriette L.; Fangel, Jonatan U.; McCleary, Barry
- Journal of Biological Chemistry, Vol. 287, Issue 47
The timing of eukaryotic evolution: Does a relaxed molecular clock reconcile proteins and fossils?
journal, October 2004
- Douzery, E. J. P.; Snell, E. A.; Bapteste, E.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 43
2-Keto-Sugar Acids in Green Flagellates: a Chemical Marker for Prasinophycean Scales1,2
journal, August 1991
- Becker, Burkhard; Becker, Dieter; Kamerling, Johannis P.
- Journal of Phycology, Vol. 27, Issue 4
Basket scales of the green alga, Mesostigma viride: Chemistry and ultrastructure
journal, October 1991
- Domozych, David S.; Wells, Brian; Shaw, Peter J.
- Journal of Cell Science, Vol. 100, Issue 2
4-O-methylation of glucuronic acid in Arabidopsis glucuronoxylan is catalyzed by a domain of unknown function family 579 protein
journal, August 2012
- Urbanowicz, B. R.; Pena, M. J.; Ratnaparkhe, S.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 35
Glycosyl transferases in family 61 mediate arabinofuranosyl transfer onto xylan in grasses
journal, January 2012
- Anders, N.; Wilkinson, M. D.; Lovegrove, A.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 3
Evidence That GH115 α-Glucuronidase Activity, Which Is Required to Degrade Plant Biomass, Is Dependent on Conformational Flexibility
journal, November 2013
- Rogowski, Artur; Baslé, Arnaud; Farinas, Cristiane S.
- Journal of Biological Chemistry, Vol. 289, Issue 1
Generation and structural validation of a library of diverse xyloglucan-derived oligosaccharides, including an update on xyloglucan nomenclature
journal, January 2015
- Tuomivaara, Sami T.; Yaoi, Katsuro; O’Neill, Malcolm A.
- Carbohydrate Research, Vol. 402
β-d-(1→4), β-d-(1→3) ‘mixed linkage’ xylans from red seaweeds of the order Nemaliales and Palmariales
journal, June 2011
- Viana, Adriano G.; Noseda, Miguel D.; Gonçalves, Alan G.
- Carbohydrate Research, Vol. 346, Issue 8
The structure and biochemistry of charophycean cell walls: I. Pectins of Penium margaritaceum
journal, November 2006
- Domozych, D. S.; Serfis, A.; Kiemle, S. N.
- Protoplasma, Vol. 230, Issue 1-2
Overexpression of a BAHD Acyltransferase, OsAt10 , Alters Rice Cell Wall Hydroxycinnamic Acid Content and Saccharification
journal, February 2013
- Bartley, Laura E.; Peck, Matthew L.; Kim, Sung-Ryul
- Plant Physiology, Vol. 161, Issue 4
Enzymatic Basis for N -Glycan Sialylation : STRUCTURE OF RAT α2,6-SIALYLTRANSFERASE (ST6GAL1) REVEALS CONSERVED AND UNIQUE FEATURES FOR GLYCAN SIALYLATION
journal, October 2013
- Meng, Lu; Forouhar, Farhad; Thieker, David
- Journal of Biological Chemistry, Vol. 288, Issue 48
The Glycosyltransferase Repertoire of the Spikemoss Selaginella moellendorffii and a Comparative Study of Its Cell Wall
journal, May 2012
- Harholt, Jesper; Sørensen, Iben; Fangel, Jonatan
- PLoS ONE, Vol. 7, Issue 5
Biosynthesis of UDP-Xylose. Cloning and Characterization of a Novel Arabidopsis Gene Family, UXS , Encoding Soluble and Putative Membrane-Bound UDP-Glucuronic Acid Decarboxylase Isoforms
journal, December 2002
- Harper, April D.; Bar-Peled, Maor
- Plant Physiology, Vol. 130, Issue 4
Insoluble (1 → 3), (1 → 4)-β-D-glucan is a component of cell walls in brown algae (Phaeophyceae) and is masked by alginates in tissues
journal, June 2017
- Salmeán, Armando A.; Duffieux, Delphine; Harholt, Jesper
- Scientific Reports, Vol. 7, Issue 1
Monoclonal antibodies indicate low-abundance links between heteroxylan and other glycans of plant cell walls
journal, July 2015
- Cornuault, Valérie; Buffetto, Fanny; Rydahl, Maja G.
- Planta, Vol. 242, Issue 6
Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation
journal, May 2014
- Hori, Koichi; Maruyama, Fumito; Fujisawa, Takatomo
- Nature Communications, Vol. 5, Issue 1
Arabidopsis thaliana IRX10 and two related proteins from psyllium and Physcomitrella patens are xylan xylosyltransferases
journal, September 2014
- Jensen, Jacob Krüger; Johnson, Nathan Robert; Wilkerson, Curtis Gene
- The Plant Journal, Vol. 80, Issue 2
Two Arabidopsis proteins synthesize acetylated xylan in vitro
journal, September 2014
- Urbanowicz, Breeanna R.; Peña, Maria J.; Moniz, Heather A.
- The Plant Journal, Vol. 80, Issue 2
Polysaccharide Analysis Using Carbohydrate Gel Electrophoresis: A Method to Study Plant Cell Wall Polysaccharides and Polysaccharide Hydrolases
journal, January 2002
- Goubet, Florence; Jackson, Peter; Deery, Michael J.
- Analytical Biochemistry, Vol. 300, Issue 1
The ability of land plants to synthesize glucuronoxylans predates the evolution of tracheophytes
journal, November 2011
- Kulkarni, Ameya R.; Peña, Maria J.; Avci, Utku
- Glycobiology, Vol. 22, Issue 3
Three Members of the Arabidopsis Glycosyltransferase Family 8 Are Xylan Glucuronosyltransferases
journal, June 2012
- Rennie, Emilie A.; Hansen, Sara Fasmer; Baidoo, Edward E. K.
- Plant Physiology, Vol. 159, Issue 4
Arabidopsis genes IRREGULAR XYLEM (IRX15) and IRX15L encode DUF579-containing proteins that are essential for normal xylan deposition in the secondary cell wall: DUF579 and xylan biosynthesis
journal, February 2011
- Brown, David; Wightman, Raymond; Zhang, Zhinong
- The Plant Journal, Vol. 66, Issue 3
Fluorescent labeling of pectic oligosaccharides with 2-aminobenzamide and enzyme assay for pectin
journal, June 2002
- Ishii, Tadashi; Ichita, Junji; Matsue, Hajime
- Carbohydrate Research, Vol. 337, Issue 11
XAX1 from glycosyltransferase family 61 mediates xylosyltransfer to rice xylan
journal, October 2012
- Chiniquy, D.; Sharma, V.; Schultink, A.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 42